Efficient production of infectious viruses requires enzymatic activity of Epstein-Barr virus protein kinase

Virology

Volumn 389, Issue 1-2, 2009, Pages 75-81

  Murata, Takayuki ^a   Isomura, Hiroki ^a   Yamashita, Yoriko ^b   Toyama, Shigenori ^a,c   Sato, Yoshitaka ^a   Nakayama, Sanae ^a   Kudoh, Ayumi ^a   Iwahori, Satoko ^a   Kanda, Teru ^a   Tsurumi, Tatsuya ^a,c  

^a AICHI CANCER CENTER HOSPITAL   (Japan)

^b NAGOYA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^c NAGOYA CITY UNIVERSITY   (Japan)

Author keywords

BGLF4; EBV; Infectivity; Protein kinase

Indexed keywords

GENE PRODUCT; PROTEIN BGLF4; PROTEIN KINASE; UNCLASSIFIED DRUG; VIRUS DNA; VIRUS ENZYME;

ARTICLE; CELL STRAIN HEK293; CONTROLLED STUDY; DNA REPLICATION; ENZYME ACTIVITY; EPSTEIN BARR VIRUS; HUMAN; HUMAN CELL; KNOCKOUT GENE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVERTANT; VIRUS GENOME; VIRUS INFECTIVITY; VIRUS MUTANT; VIRUS REPLICATION; WILD TYPE;

CELL LINE; DNA REPLICATION; DNA, VIRAL; EPSTEIN-BARR VIRUS INFECTIONS; GENE KNOCKOUT TECHNIQUES; GENETIC COMPLEMENTATION TEST; GENOME, VIRAL; HERPESVIRUS 4, HUMAN; HUMANS; PROTEIN-SERINE-THREONINE KINASES; VIRAL PROTEINS; VIRUS REPLICATION;

HUMAN HERPESVIRUS 4;

EID: 67349265475     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2009.04.007     Document Type: Article

References (38)

1. Asai R., Kato A., Kato K., Kanamori-Koyama M., Sugimoto K., Sairenji T., Nishiyama Y., and Kawaguchi Y. Epstein-Barr virus protein kinase BGLF4 is a virion tegument protein that dissociates from virions in a phosphorylation-dependent process and phosphorylates the viral immediate-early protein BZLF1. J. Virol. 80 11 (2006) 5125-5134
2. Chen M.R., Chang S.J., Huang H., and Chen J.Y. A protein kinase activity associated with Epstein-Barr virus BGLF4 phosphorylates the viral early antigen EA-D in vitro. J. Virol. 74 7 (2000) 3093-3104
3. Daikoku T., Kudoh A., Sugaya Y., Iwahori S., Shirata N., Isomura H., and Tsurumi T. Postreplicative mismatch repair factors are recruited to Epstein-Barr virus replication compartments. J. Biol. Chem. 281 16 (2006) 11422-11430
4. Delecluse H.J., Hilsendegen T., Pich D., Zeidler R., and Hammerschmidt W. Propagation and recovery of intact, infectious Epstein-Barr virus from prokaryotic to human cells. Proc. Natl. Acad. Sci. U. S. A. 95 14 (1998) 8245-8250
5. Gershburg E., Raffa S., Torrisi M.R., and Pagano J.S. Epstein-Barr virus-encoded protein kinase (BGLF4) is involved in production of infectious virus. J. Virol. 81 10 (2007) 5407-5412
6. Isomura H., Tsurumi T., and Stinski M.F. Role of the proximal enhancer of the major immediate-early promoter in human cytomegalovirus replication. J. Virol. 78 23 (2004) 12788-12799
7. Isomura H., Stinski M.F., Kudoh A., Murata T., Nakayama S., Sato Y., Iwahori S., and Tsurumi T. Noncanonical TATA sequence in the UL44 late promoter of human cytomegalovirus is required for the accumulation of late viral transcripts. J. Virol. 82 4 (2008) 1638-1646
8. Kanda T., Yajima M., Ahsan N., Tanaka M., and Takada K. Production of high-titer Epstein-Barr virus recombinants derived from Akata cells by using a bacterial artificial chromosome system. J. Virol. 78 13 (2004) 7004-7015
9. Kato K., Kawaguchi Y., Tanaka M., Igarashi M., Yokoyama A., Matsuda G., Kanamori M., Nakajima K., Nishimura Y., Shimojima M., Phung H.T., Takahashi E., and Hirai K. Epstein-Barr virus-encoded protein kinase BGLF4 mediates hyperphosphorylation of cellular elongation factor 1delta (EF-1delta): EF-1delta is universally modified by conserved protein kinases of herpesviruses in mammalian cells. J. Gen. Virol. 82 Pt 6 (2001) 1457-1463
10. Kato K., Yokoyama A., Tohya Y., Akashi H., Nishiyama Y., and Kawaguchi Y. Identification of protein kinases responsible for phosphorylation of Epstein-Barr virus nuclear antigen leader protein at serine-35, which regulates its coactivator function. J. Gen. Virol. 84 Pt 12 (2003) 3381-3392
11. Kato A., Yamamoto M., Ohno T., Tanaka M., Sata T., Nishiyama Y., and Kawaguchi Y. Herpes simplex virus 1-encoded protein kinase UL13 phosphorylates viral Us3 protein kinase and regulates nuclear localization of viral envelopment factors UL34 and UL31. J. Virol. 80 3 (2006) 1476-1486
12. Kawaguchi Y., and Kato K. Protein kinases conserved in herpesviruses potentially share a function mimicking the cellular protein kinase cdc2. Rev. Med. Virol. 13 5 (2003) 331-340
13. Kawaguchi Y., Kato K., Tanaka M., Kanamori M., Nishiyama Y., and Yamanashi Y. Conserved protein kinases encoded by herpesviruses and cellular protein kinase cdc2 target the same phosphorylation site in eukaryotic elongation factor 1delta. J. Virol. 77 4 (2003) 2359-2368
14. Krosky P.M., Baek M.C., and Coen D.M. The human cytomegalovirus UL97 protein kinase, an antiviral drug target, is required at the stage of nuclear egress. J. Virol. 77 2 (2003) 905-914
15. Kudoh A., Fujita M., Kiyono T., Kuzushima K., Sugaya Y., Izuta S., Nishiyama Y., and Tsurumi T. Reactivation of lytic replication from B cells latently infected with Epstein-Barr virus occurs with high S-phase cyclin-dependent kinase activity while inhibiting cellular DNA replication. J. Virol. 77 2 (2003) 851-861
16. Kudoh A., Daikoku T., Ishimi Y., Kawaguchi Y., Shirata N., Iwahori S., Isomura H., and Tsurumi T. Phosphorylation of MCM4 at sites inactivating DNA helicase activity of the MCM4-MCM6-MCM7 complex during Epstein-Barr virus productive replication. J. Virol. 80 20 (2006) 10064-10072
17. Lake C.M., and Hutt-Fletcher L.M. The Epstein-Barr virus BFRF1 and BFLF2 proteins interact and coexpression alters their cellular localization. Virology 320 1 (2004) 99-106
18. Lee C.P., Chen J.Y., Wang J.T., Kimura K., Takemoto A., Lu C.C., and Chen M.R. Epstein-Barr virus BGLF4 kinase induces premature chromosome condensation through activation of condensin and topoisomerase II. J. Virol. 81 10 (2007) 5166-5180
19. Lee C.P., Huang Y.H., Lin S.F., Chang Y., Chang Y.H., Takada K., and Chen M.R. Epstein-Barr virus BGLF4 kinase induces disassembly of the nuclear lamina to facilitate virion production. J. Virol. 82 23 (2008) 11913-11926
20. Morrison E.E., Wang Y.F., and Meredith D.M. Phosphorylation of structural components promotes dissociation of the herpes simplex virus type 1 tegument. J. Virol. 72 9 (1998) 7108-7114
21. Murata T., and Shimotohno K. Ubiquitination and proteasome-dependent degradation of human eukaryotic translation initiation factor 4E. J. Biol. Chem. 281 30 (2006) 20788-20800
22. Murata T., Sato Y., Nakayama S., Kudoh A., Iwahori S., Isomura H., Tajima M., Hishiki T., Ohshima T., Hijikata M., Shimotohno K., and Tsurumi T. TORC 2, a coactivator of CREB, promotes Epstein-Barr virus reactivation from latency through interaction with viral BZLF1 protein. J. Biol. Chem. 284 12 (2009) 8033-28041
23. Ng T.I., Chang Y.E., and Roizman B. Infected cell protein 22 of herpes simplex virus 1 regulates the expression of virion host shutoff gene U(L)41. Virology 234 2 (1997) 226-234
24. Ogle W.O., and Roizman B. Functional anatomy of herpes simplex virus 1 overlapping genes encoding infected-cell protein 22 and US1.5 protein. J. Virol. 73 5 (1999) 4305-4315
25. Overton H.A., McMillan D.J., Klavinskis L.S., Hope L., Ritchie A.J., and Wong-kai-in P. Herpes simplex virus type 1 gene UL13 encodes a phosphoprotein that is a component of the virion. Virology 190 1 (1992) 184-192
26. Polack A., Hortnagel K., Pajic A., Christoph B., Baier B., Falk M., Mautner J., Geltinger C., Bornkamm G.W., and Kempkes B. c-myc activation renders proliferation of Epstein-Barr virus (EBV)-transformed cells independent of EBV nuclear antigen 2 and latent membrane protein 1. Proc. Natl. Acad. Sci. U. S. A. 93 19 (1996) 10411-10416
27. Purves F.C., Ogle W.O., and Roizman B. Processing of the herpes simplex virus regulatory protein alpha 22 mediated by the UL13 protein kinase determines the accumulation of a subset of alpha and gamma mRNAs and proteins in infected cells. Proc. Natl. Acad. Sci. U. S. A. 90 14 (1993) 6701-6705
28. Reynolds A.E., Ryckman B.J., Baines J.D., Zhou Y., Liang L., and Roller R.J. U(L)31 and U(L)34 proteins of herpes simplex virus type 1 form a complex that accumulates at the nuclear rim and is required for envelopment of nucleocapsids. J. Virol. 75 18 (2001) 8803-8817
29. Tanaka M., Nishiyama Y., Sata T., and Kawaguchi Y. The role of protein kinase activity expressed by the UL13 gene of herpes simplex virus 1: the activity is not essential for optimal expression of UL41 and ICP0. Virology 341 2 (2005) 301-312
30. Tarakanova L., Leung-Pineda V., Hwang S., Yang C.W., Matatall K., Basson M., Sun R., Piwnica-Worms H., Sleckman B.P., and Virgin H.W.t. Gamma-herpesvirus kinase actively initiates a DNA damage response by inducing phosphorylation of H2AX to foster viral replication. Cell. Host. Microbe. 1 4 (2007) 275-286
31. Tsurumi T. Purification and characterization of the DNA-binding activity of the Epstein-Barr virus DNA polymerase accessory protein BMRF1 gene products, as expressed in insect cells by using the baculovirus system. J. Virol. 67 3 (1993) 1681-1687
32. Tsurumi T., Kobayashi A., Tamai K., Daikoku T., Kurachi R., and Nishiyama Y. Functional expression and characterization of the Epstein-Barr virus DNA polymerase catalytic subunit. J. Virol. 67 8 (1993) 4651-4658
33. Tsurumi T., Fujita M., and Kudoh A. Latent and lytic Epstein-Barr virus replication strategies. Rev. Med. Virol. 15 1 (2005) 3-15
34. van Zeijl M., Fairhurst J., Baum E.Z., Sun L., and Jones T.R. The human cytomegalovirus UL97 protein is phosphorylated and a component of virions. Virology 231 1 (1997) 72-80
35. Wang J.T., Yang P.W., Lee C.P., Han C.H., Tsai C.H., and Chen M.R. Detection of Epstein-Barr virus BGLF4 protein kinase in virus replication compartments and virus particles. J. Gen. Virol. 86 Pt 12 (2005) 3215-3225
36. Wolf D.G., Courcelle C.T., Prichard M.N., and Mocarski E.S. Distinct and separate roles for herpesvirus-conserved UL97 kinase in cytomegalovirus DNA synthesis and encapsidation. Proc. Natl. Acad. Sci. U. S. A. 98 4 (2001) 1895-1900
37. Yang P.W., Chang S.S., Tsai C.H., Chao Y.H., and Chen M.R. Effect of phosphorylation on the transactivation activity of Epstein-Barr virus BMRF1, a major target of the viral BGLF4 kinase. J. Gen. Virol. 89 Pt 4 (2008) 884-895
38. Yue W., Gershburg E., and Pagano J.S. Hyperphosphorylation of EBNA2 by Epstein-Barr virus protein kinase suppresses transactivation of the LMP1 promoter. J. Virol. 79 9 (2005) 5880-5885